MuriquiBrachyteles

SOCIAL ORGANIZATION AND BEHAVIOR

In addition to affecting their diet, the geographic dispersal of resources
influences the grouping patterns and social structure of muriquis. At the two
study sites where muriquis have been studied systematically, Montes Claros and
Barreiro Rico, the structure of social groups varies (Strier 1987b). At Montes
Claros, where large fruiting trees are more abundant and closely spaced, muriquis
live in social groups of 20 to more than 80 individuals which travel and feed together
throughout the day. In contrast to the large social groups present at Montes
Claros, muriquis live in small groups at Barreiro Rico, where fruit trees are
scarcer and widely dispersed. The only permanent associations at this site are
between adult females and their offspring, and social groups consist of three to
five adult females and their dependent offspring. These units travel alone and
are joined, on occasion, by subadult and adult males (Milton 1984). The female
groups remain in discrete home ranges. The males travel alone or in groups of
up to eight individuals, joining different groups of females for short periods
to mate and then moving on to find other
estrous females.
Associations between adult males and females at Barreiro Rico last between a few
minutes to over a week (Milton 1984).

The abundance of feeding sites at Montes Claros might allow larger groups to
form and stay together without costly competition for resources at feeding sites
(Strier 1989; Strier et al. 1993). In fact, after several years of growth
resulting in an almost doubling of group size, the study group at Montes Claros
shifted its behavior from maintaining a large, cohesive group, to two smaller
groups that come together often, but frequently travel separately. Unlike the
small groups at Barreiro Rico, the groups come together regardless of female
receptivity (Strier et al. 1993). This change in behavior was accompanied by a
widening of the home range size, indicating that there is a positive relationship
between resource availability and muriqui social group size and home range size
(Strier 1989; Dias & Strier 2003). As of 2006, there were four muriqui
groups in this forest and a total population of 226 individuals (Strier et al. 2006).

Information about the social structure of muriquis comes chiefly from the
long-term research at Montes Claros. Muriquis exhibit
male philopatry,
staying in the groups where they were born while females leave their
natal groups
between five and seven years of age to join another group, where they
will stay and mate for life (Strier 1991b; 1996). Young females often leave
their natal group shortly after an agonistic
encounter with a neighboring group (Strier 1993). They are not forced out by
older females, as is seen in some other primates such as the
callitrichines,
but seem to part from their group amicably (Strier & Ziegler 2000).
Aggression in muriquis is exceptionally rare, but when a female attempts to
join a social group, she is chased and displaced by the adult females in the
group (Strier 1991b; 1992b). Adult resident females frequently displace young
immigrants at quality feeding sites and young females remain on the periphery
of the social group (Printes & Strier 1999). Young female immigrant
muriquis gain acceptance by playing and interacting with juvenile or subadult
females of the group, and eventually the adult females will tolerate their
presence (Strier 1991b; 1992b; 1996).

Males within the same group are likely to be related, because of the dispersal
patterns exhibited by muriquis, and do not behave agonistically
to one another, even in the presence of reproductive females (Strier et al. 2002).
There is little evidence of dominance relationships either between females,
between males, or between females and males (Strier 1992b). Embracing or
affiliative
hugging is one way in which social relationships are strengthened among male
muriquis while social grooming is rare (Strier 1994; Strier et al. 2002).
Though muriquis of the same group have
egalitarian
relationships, interactions between males of neighboring groups are hostile.
Vocal displays, threat displays, and chasing characterize interactions between
males of two groups which come into contact with one another. This agonistic
behavior may be to prevent intruder males from coming into contact with
females of a social group (Strier 1994). Related males of a social group work
together to keep strange males from entering the group; when males cannot prevent
outsiders from coming into contact with females, the new males often
copulate
with group females (Strier 1994).

REPRODUCTION

Muriquis are promiscuous and exhibit a
polygamous mating system
in which both males and females mate with multiple partners (Milton 1985; Strier
1986). At Montes Claros, females mate with an average of eight different males
during the mating season and males mate with an average of 14 different females
(Strier 1997). Mating is concentrated during the months from September through
March and births occur primarily during the peak dry months, June through
August (Strier 1991b; 1996; 1997). Reproduction is correlated with rainfall and
thus availability of new leaves, an important food source for muriquis after
the dry season shortages (Strier 1996). In the dry season, when day ranges
are shorter, muriqui mothers with highly dependant infants may benefit because
they do not have to expend extra energy traveling long distances while carrying
an infant. As fruiting begins, the infant has grown and is less awkward to
carry because it is larger and has more strength and the female can travel the
longer distances seen during the wet season (Strier 1986; 1996).

Females reach puberty after transferring from their natal group and experience a
delay in the normalization of their
ovarian cycle
which lasts about 14 months after transferring, or at least one breeding season
(Strier & Ziegler 2000). Females do not cycle throughout the year but
rather only during the mating season (Strier &
Ziegler 1994). The ovarian cycle lasts an average of 21 days, but can range
between 16 and 38 days, and there are no external signs of
ovulation
(Strier & Ziegler 1997). Females copulate at 20 day intervals during the
mating season and may mate over several
reproductive cycles (Strier & 1997). The age at first reproduction for females
has only been documented in only a few females whose birth dates are known and
occurs between 7.5 and nine years of age (Strier 1996; Martins & Strier 2004).
Gestation
lasts about seven months (averaging 216 days) and there is a long
interbirth
interval, averaging 36 months (Strier 1996; Strier & Ziegler 1997).

Males begin to reproduce around five or six years of age (Strier 1996).
Aggression or physical competition for access to mates has not been documented
among muriquis, and one hypothesis is that physical adaptations in males reduce
the need for overt competition and instead, sperm competition is practiced
(Strier 1992a; 1997). Male muriquis have large testicles compared to their
body size and larger testes result in higher levels of sperm production (Strier
1992a). Among animals in which males and females mate with multiple partners,
there is potentially an advantage to a male that can produce the largest amount
of sperm; he has a higher chance of successfully fertilizing a female compared
to other males (Dixson & Anderson 2002).

PARENTAL CARE

Infants are born with light fur and dark faces and they begin to lose their
natal coat
and skin pigmentation between three and four years of age. They do not reach
adult size until they are between five and seven years of age (Strier 1993).
Female muriquis are the sole caregivers of their offspring, carrying and nursing
their infants as they slowly gain independence and are eventually weaned (Strier
1993). Adult males have been characterized as indifferent to infants within
their group and rarely come into contact with them. Interactions are friendly
but brief, and are always initiated by the infants (da Oliveira Guimarães &
Strier 2001).

For the first year of life, muriqui infants are almost fully dependent on their
mother for transportation and food. During the first six months, the infant
clings to the fur on its mother's belly and sides and is awkward to carry for
the mother. As the infant matures, it begins to ride jockey-style on its
mother's back, wrapping its
prehensile tail
around its mother's tail for added support (Strier 1992a; 1993). The two remain
in almost constant contact during the early months, and gradually decrease
contact time. The mother may leave her infant on a thin branch while she
feeds next to it but will always gather it up before moving to the next feeding
or resting site. Six to 12-month old infants are never more than a few feet
from their mothers, and spend time tentatively exploring while their mother is
feeding or resting (Strier 1992a).

After the first year, young muriquis gain more independence from their mothers
and are able to travel short distances without the help of their mother.
Groups of infants are often parked together and socialize through play while
the mothers feed (Strier 1992a). In some instances, young muriquis require
the assistance of their mothers to negotiate large gaps in the canopy. In
these cases, the mother will form a bridge, using her long, prehensile tail
and her front legs, stretching the length of the gap and allowing her young
to cross over her (Strier 1992a).

Weaning
occurs between 18 and 24 months, though experimentation with solid foods occurs
months before. The weaning process is often a traumatic time for the juvenile
muriqui. Mothers refuse nursing attempts of their juvenile offspring by hitting
or nipping at them when they try to suckle, and young muriquis may throw tantrums,
screeching and whining until they are allowed to nurse or grow tired (Strier
1991b; 1992a). Young muriquis begin to
forage
completely on their own at around two years of age (Strier 1992a). In the
breeding season after her infant is weaned, the mother will begin to copulate
and will likely conceive. The interbirth interval is about 36 months, but the
average interval between
parturition
and resumption of copulation is 23.5 months (Strier 1996). A young muriqui is
about three years old when its sibling is born, and by this time is completely
independent from its mother (Strier 1992a).

COMMUNICATION

Muriquis communicate through vocalizations, postural behavior, and chemical
communication. One common vocal call is the "neigh," which is a loud,
horse-like call given frequently in the early morning, during travel, and
at the end of the day before entering the sleeping tree. One function may
be to inform other animals of an individual's location and maintaining group
unity throughout the day when muriquis cannot see one another (Torres de
Assumpção 1984; Strier 1986; Nishimura et al. 1988). It may also
serve as a spacing function for other muriqui groups in the area,
communicating the location of the one group to another (Strier 1986). When
two muriqui groups come into contact, the most common vocalization is the
"bark." Much like the hoarse-sounding bark of a dog, adult male and female
muriquis bark at two- to three-second intervals before, during, and after an
intergroup encounter (Milton 1984; Strier 1986; Nishimura et al. 1988). Mild
anxiety among muriquis is expressed by "hoots," and can be heard after long
barking bouts. Females traveling with young can be heard giving "cluck" calls,
a soft smacking call that may be a reassuring sound to infants or juveniles left
in one part of the tree while the mother forages elsewhere in the tree (Strier
1986). The common feeding call given by both adult males and females is the
"chirp." Infants and juveniles make calls when they are upset, during weaning
and when they are left behind by the group. These include "screams" and
"whines," both of which usually result in a response from their mothers
(Strier 1986).

Some vocalizations are accompanied by physical displays. Adult male muriquis
often embrace both as a friendly gesture and during times of extreme excitement.
"Clucks" are given during friendly embraces, but sometimes embracing escalates
when males are agitated, such as after an intergroup encounter, and several
males will frantically embrace each other and emit "warbles," throaty
gurgling calls (Strier 1986). Another greeting gesture seen between adult
males and adult females, but not between members of the opposite sex, is a
ritualized embrace in which the two animals emit "staccato chutter-whinnies"
and hug forcefully, both animals pulling their lips back over their teeth into
a grimace (Milton 1984). Other display behaviors include slapping leaves and
branches with the hands, forcefully pulling branches back and letting them go,
lunging, and defecating (Milton 1984).

Adult male and female muriquis use chemical communication to convey sexual
receptivity and interest to members of the opposite sex. Both males and
females communicate via urine washing; they urinate directly onto the hands,
feet, or tail, and rest the coated appendage on branches, leaving a trail as
they walk or hang by their tails for other animals to encounter (Milton 1985).

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